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CHAPTER 10
Parasitism in man-made ecosystems
François Renaud,1 Thierry De Meeüs,1 and Andrew F. Read2
Technological and cultural change in human populations is opening up new
ecological niches for pathogens and parasites. The organisms that cause
many of these ‘‘diseases of progress’’ have opportunities for global spread and
access to host population densities unprecedented in human history.
Understanding the natural history and evolutionary ecology of these
pathogens needs to become a key part of public health planning.
10.1 Introduction
Like free-living organisms, parasites and pathogens
can colonize and evolve in new environments. In this
way, travel and technical developments (e.g. air conditioning, plane, boats, new economic links, etc.),
medical and surgical developments (e.g. catheters,
fibroscopy, prosthesis, organ transplants associated
with anti-rejection medicine, immunosuppressive
drugs, etc.) are generating new environments in
hospital ecosystems which are colonized now by new
parasite and pathogen flocks. Elsewhere, agricultural
processes have widely disturbed ecological parameters in natural ecosystems for food development;
they are responsible for the emergence and development of new parasite and pathogen species, and also
for changes in host–parasite interactions. Through
different examples, the aim of this chapter is to present and to discuss some phenomena and processes
involved in the conquest by parasites and pathogens
of man-made ecosystems. We could name diseases
which are the result of pathogens colonizing manmade ecosystems as ‘progress infectious diseases’.
To pass from 6 billion to 10 or 12 billion human
inhabitants by the end of the twenty-first century
1
Génétique et Evolution de Maladies Infectieuses GEMI/UMR
CNRS-IRD 2724, Equipe: ‘Evolution des Systèmes Symbiotiques’,
IRD, 911 Avenue Agropolis, B.P. 5045, 34032 Montpellier Cedex 1,
France.
2
Institutes of Evolution, Immunology and Infection Research,
School of Biological Sciences, University of Edinburgh, EH9 3JT,
Scotland.
represents one main subject of anxiety for scientists.
Ten billion humans could not live on the earth with
the lifestyle enjoyed by the 750 million people
presently living in developed countries, because of
lack of water, energy, quality, and quantity of space.
Developed countries must contribute to the development of all countries to balance economy and life
conditions. However (indeed, if ever) this is
achieved, substantial environmental modification
seems likely. Throughout history, mankind has
severely modified the biosphere. Human impacts on
ecosystems are as old as the human species.
However, following industrialisation, the consequent increase in numbers of people and their ability
to modify the biosphere, the extent and consequences of human impacts on ecosystems have
accelerated. Impacts resulting from human activities
occur in all parts of the biosphere, and at all kinds of
temporal and spatial scales. (Dickinson and Murphy
1998). The ecological consequences of the unavoidable modifications of the future are hard to predict:
we simply do not have a thorough understanding of
the impact of global change on local environmental
conditions and the evolution of biodiversity.
10.1.1 But what is an ecosystem?
Let us imagine a pond, for example. What animals
might live here? Insects, worms, birds, fish, mice,
muskrats, ducks, deer, wolves. What do these
animals need to eat? Insects eat plants, fish eat
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worms and insects, birds eat fish, worms, and
insects. Mice eat grain. Muskrats eat ducks, eggs,
and chicks. Ducks eat insects and worms. Deer eat
grass. Wolves eat mice, muskrats, and deer. All
these animals rely on the pond for the water they
need. The deer cut the grass, wolves remove the
sick and weak deer from the herd. Muskrats regulate the duck population. All these animals rely on
each other. Just like people in a human community.
An ecosystem is a community too. Consider a pond
community, with all its variety of plants, insects,
birds, and other living things. What would happen
to the community if the water vanished? What if
the ducks all disappeared?
Other examples of ecosystems include forests,
rivers, oceans, deserts, cold arctic tundra, high
mountains, and rain forests. Different plants and
animals grow in different ecosystems. Normally,
the living things in the ecosystem balance in such
a way that no living things take over the whole
ecosystem and destroy it, at least not for a while.
For example, the production of O2 by the first photosynthetic algae had dramatic consequences on
the anaerobic life that predominated at that time.
10.1.2 But why some deer are sick and weak
within the herd?
May be they could be parasitized? We just want to
underline here that the above description of an
ecosystem, as we can read it in numerous books or
websites, disregards systematically the fundamental
role that parasites play in ecosystem functioning!
Indeed, it is less poetic to speak about a tapeworm or
a virus than a duck or a deer! Nevertheless, parasites
are present in a large part of ecosystems, and the liver,
kidneys, lungs, gills, gut, and pharyngeal sphere of a
host constitute as many ecosystems for parasites
and pathogens as do rivers, oceans, desert, high
mountains, and jungles for free-living organisms.
10.1.3 But what is a parasite and/or a
pathogen?
‘An organism in or on another living organism
obtaining from it part or all of its organic nutriments,
commonly exhibiting some degree of adaptive
structural modifications, and causing some degree of
real damage to its host’ (Price 1980). So, the parasite/
pathogen lives at the expense of the host, and this
host’s exploitation has automatic consequences on
host biology and physiology, on host evolutionary
biology and on evolutionary relationships between
hosts and parasites (Renaud and De Meeüs 1991).
Because the host represents the ‘habitat/resource’
system of the parasite, each modification on host
ecosystem will have consequences on the parasite
ecosystem, and because parasites affect host fitness,
they act on host ecosystem too. Because living organisms are parasitized, we cannot consider ecosystem
evolution without parasites (see Chapter 9).
It is undeniable that humans greatly disturb
ecosystem equilibrium (deforestation, eutrophication, overgrazing, etc.), but the aim of this chapter
is not to consider anthropogenic ecosystem disturbances and subsequent evolution of parasites and
diseases which are presented in other chapters of
this book (see Chapter 7). Instead, we will illustrate
and discuss, through different examples, the impact
of technical progress by humans on the evolutionary ecology of parasites and pathogens. How have
parasites exploited new ‘human-made’ ecosystems,
especially those concerning public health?
10.1.4 What is a ‘human made’ ecosystem?
It is an ecosystem artificially elaborated by humans
in order to enhance their quality of life.
For example, let us imagine that the wheel was
never invented! The wheel is everywhere on our
cars, trains, planes, machines, wagons, and most factory and farm equipment. What could we do without wheels? But as important the wheel is, we do not
know who exactly invented it. The oldest wheel
found in archaeological excavations was discovered
in Mesopotamia, and is believed to be more than
5500 years old. Eventually, wheels became covered
with tyre in order to make the trip more easy and
pleasant. But, it is almost impossible remove all the
water a worn-out tyre contains. Consequently, old
tyres become excellent habitat for the larvae of different mosquito species, especially Aedes spp. which
are the vectors of the Dengue virus. Worn and waste
tyres are being traded throughout the world, and are
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3
1
2
Figure 10.1 Example of hypothetical main routes of Aedes albopictus- infested tires.
Notes: 1: Japanese origin; 2: first colonization wave: US and South America in 1985/1986; 3: second colonization wave: Mexico, Africa, and Europe in
1990/1991.
Source: Data from Reiter (1998: 93, table 10).
responsible for the introduction of mosquitoes in
different countries (Fig. 10.1). ‘In short, it seems we
must accept the establishment of exotic species as an
inevitable consequence of modern transportation
technology’ (Reiter 1998). For example, inspections
of containers arriving in US ports showed the presence of living Aedes albopictus and four other mosquito species in worn tyres from Japan (Craven et al.
1988). Japan is the biggest exporter of worn tyres in
the world. Ae. albopictus is capable of vertical and
horizontal transmission of the Dengue virus, and
other important human arboviruses (Shroyer 1986).
Thus pathogenic agents can take advantage of tyre
trade. We can imagine that such trades could have
also consequences on other vectors, such as the
Anopheles mosquitoes which transmit malaria.
10.2 Economic and touristic human
travels: enhancement of human contacts!
Boats not only carry the worn tyres which constitute
new ecosystems for mosquito larvae, but they also
have bilge. The classic bacterial disease, cholera,
entered both North and South America during the
last century from the bilge-water of an Asian
freighter. Indeed, molecular typing showed that the
South American isolates were pandemic genotypes
previously observed in Asia. Water bilge seems to
constitute a very good ecosystem for the transported pathogens such as bacteria (Anderson 1991;
Morse 1995). Cholera is not the only opportunistic
pathogen which use such kinds of transport: an epidemic strain of Neisseria meningitidis seems to have
disseminated rapidly along routes by travelling in
ballast waters (Moore and Broome 1994).
Malaria parasites use mosquitoes to transmit
between vertebrate hosts. For example, different
mosquito species belonging to the genus Anopheles
are the definitive hosts of the malaria agent
Plasmodium vivax , one of the four species of human
malaria. Human malaria is currently absent in
western Europe, but an autochthonous case of P.
vivax malaria occurred in Tuscany (Italy) in August
1997, decades after malaria eradication (Baldari et al.
1998)! The disease was diagnosed in a woman with
no travel history who lived in a rural area where
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indigenous Anopheles labranchiae, the former main
malaria vector in Italy, was abundant (Romi et al.
1997). A molecular epidemiological investigation
concluded that this was an introduced malaria case,
and indicated a girl recently immigrated from
Punjab (India) and living about 500 m away from
the patient, as the source of P. vivax infection
(Severini et al. 2002). The parasite was able to pass
from Asia to Europe because an infected host took
a plane to visit a family member. Planes and boats
constitute new opportunities for vector and
pathogen dispersion, in the same way as when
a pathogen is using different hosts for its dispersal.
Parasites and pathogens are able to colonise new
environments and to adapt locally to new hosts and
vectors through human-made transportation.
Similarly, epidemics of malaria in NE Brazil in the
1930s occurred because of the introduction of
Anopheles gambiae , one of the most efficient malaria
vectors, which probably arrived from a boat bringing mail from Africa (Killeen et al. 2002).
But what could be the consequences ever more
frequent travel? What would be the possible
(a)
consequences on pathogens evolution as regards to
resistance and virulence? Vector-borne diseases
such as malaria and water-borne diseases such as
cholera are generally more virulent than diseases
spread by direct infection (Ewald 1994). One reason
for this may be that vector or water-borne diseases
to spread over long distances, and causing infection
of susceptible individuals distant from the infected
individual. In a spatially structured host population, the ability of the pathogen to infect distant
individuals leads to the evolution of a more virulent pathogen (Boots and Sasaki 1999). Developing
travel alters the connections between different
towns or areas (Fig. 10.2). We could have passed
from a regular lattice between the different points
to random net-connections which are permitted by
long and frequent travels. From their analyses on
the consequences of the modification and the evolution of connections, Watts and Strogatz (1998)
suggested that infectious diseases spread more easily in small-word networks than in ‘regular’ lattices. We can predict that the increase in world
travel would have strong consequences on
(b)
(c)
Increasing randomness
Figure 10.2 Connection topology from (a) regular ring lattice, to (b) small-world, to (c) a random network.
Notes: The intermediate connection is called ‘small world’ network, and infectious diseases spread more easily in small-world networks that in regular
lattices. The different means of transport are presented in order to try to illustrate the development of ‘travel man-made ecosystems’ which permit to
link different geographical points and modify the connections within and between populations. No company or factory could be incriminated here for
disseminating pathogens.
Source: Modified from Watts, D. J. and Strogatz, S. H. (1998).
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pathogens dispersal and consequently on the evolution of infectious diseases virulence and resistance, but this could be also applied for all
categories of vectors which are responsible of
pathogen carriages. It seems reasonable to assume
that human societies in the past lived in larger with
more isolated communities. But, modern social networks (Wasserman and Faust 1994) are known to
be small words (Watts and Strogatz 1998), and it
follows that infection networks may also show
‘small world’ connections in modern societies.
When infections occur predominantly locally we
predict a lower virulence than when transmissions
occur predominantly randomly throughout within
and between populations (Boots and Sasaki 1999).
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10.3 Human comfort and
industrialization
Throughout human evolution, people have always
tried to enhance their comfort. Temperature and
humidity have a significant effect on human comfort and health. The most comfortable humidity
range is 40–60%, but air temperature and humidity
are related in respect to comfort or perceived temperature. The combination of temperature and
humidity where people report comfort is termed
the ‘comfort zone’. At the time we are writing this
chapter, an epidemic legionnaire’s disease occurs in
North of France (Pas de Calais). Indeed, 85 persons
where infected during January and February 2004,
and among them 13 died (Fig. 10.3).
1
a
5
2
3
4
Figure 10.3 Persons exposed to Legionnaires’ disease the case of factory cooling towers which could constitute a potential reproductive ground for
Legionella bacteria, Pas de Calais—France 2004: >80 cases of Legionella disease.
Notes: 1: Technical personal intervening near the cooling towers; 2: persons working near the smoke; 3: persons living in buildings and houses near
the factory: the contaminated air penetrating through windows and new air intakes.
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Legionnaires’ disease is a lung infection
pneumonia) caused by a Legionella pneumophila.
The name of this bacterium was derived from the
original outbreak at the 1976 American Legion
Convention in Philadelphia (Hlady et al. 1993).
These bacteria are readily found in natural aquatic
environments and some species have been recovered from soil. Legionella parasitize Amoeba, and
spread through cysts of these protozoans
(Fliermans 1996). The pathogen can survive in a
wide range of conditions, including temperatures
of 0–63 °C, pH of 5.0–8.5, and dissolved oxygen
concentrations of 0.2–15 ppm in water. Temperature
is a critical determinant for Legionella proliferation.
Legionella and other micro-organisms become
attached to surfaces in an aquatic environment
forming a biofilm. Legionella has been shown to
attach to and to colonize various materials found in
water systems including plastics, rubber, and
wood. But, crucially from the public health perspective, Legionnella are not only found in natural
habitats. These bacteria develop particularly well in
human infrastructures where water is present as
saunas, for example (Den Boer et al. 1998). But the
main human-made ecosystem they colonize seems
to be the cooling systems found, for example, in factories, hotels, and hospitals (Alary and Joly 1992;
Pedro-Botet et al. 2002; Sabria and Yu 2002). For
instance, in January 2000, WorkSafe Western
Australia reported a case of Legionnaires’ disease
from a teacher who had worked in a room supplied
with cooled air from an evaporative air-conditioning
unit, and had also used potting mix while gardening at home. Both potting mix and warm water
allow multiplication of these bacteria.
Figure 10.3 describes the different steps of human
infection by Legionella. But, not only workers who
live in the contaminated building are concerned,
indeed people working or living around the
Legionella source can be infected (Fig. 10.4). For
example, during the 2004 French epidemic discussed
above, the infected patients were people living near
a factory where the bacteria were identified in the
cooling systems. Even though the link between the
presence of the bacteria and human infections was
not clearly established, the French government
decided to stop immediately the factory activity.
Other microbes can contaminate air-conditioning
units and cooling towers which can result in other
health problems for workers and visitors such as
respiratory sensitization and building related
illness, or ‘sick building syndrome’. It is thus
essential to maintain a good indoor air quality at
all times.
Water is essential for life! But drinking water
networks are heterogeneous and constitute real biological reactors, that is to say an ecosystem between
a mobile phase (i.e. water) and an appointed phase
(i.e. biofilm). These networks are continually contaminated by microorganisms (i.e. bacteria, algae,
protozoans, fungi, yeast, metazoans) and nutrients
(i.e. organic dissolved matter) that passed through
the treatment systems or gather from accidental
procedures (i.e. breaks and repairs). Drinking water
networks thus bring together all the favourable
conditions for the maintenance and the spread of
microbial systems diversified and organized in
different trophic levels, and thus constitute real
food webs.
Another example which could well illustrate the
phenomenon of disease induced by the human
desire for comfort is wastewater such as those
encountered near houses in septic tanks. Septic
tanks were designed to improve sanitation.
Bacteria, viruses, protozoans, and worms are
the types of pathogens in wastewater that are
hazardous to human. Bacteria are responsible for
several wastewater related diseases, including
typhoid, bacillary dysentery, gastroenteritis, and
cholera. Depending on the bacteria involved,
symptoms can begin hours to several days after
ingestion. Viruses cannot multiply outside their
hosts, and wastewater is a hostile environment for
them. But enough viruses survive in water to make
people sick. Hepatitis A, polio, and viral gastroenteritis are a few of the diseases that can be
contracted from viruses in wastewater. A protozoan
is the cause of amoebiosis, also known as amoebic
dysentery. Parasitic worms also dwell in untreated
sewage. Tapeworms and pinworms are the most
common parasites found in these wastewaters,
from where their eggs can be ingested. Children and
the elderly are the groups the most significantly
affected by wastewater related diseases.
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1
2
3
Figure 10.4 Legionella disease: infection routes.
Notes: 1: The pathogen responsible for the disease is a bacteria living in fresh water. The optimal growth temperature is between 35 and 40 °C. This
pathogen is present in sanitary facilities (showers, taps, etc.), air conditioning, fountains, greenhouse, cooling towers, etc. For example, bacteria are
presents in droplets coming from factory steam; 2: Bacteria contained in ‘contaminated droplets’ are inhaled by humans, and clinical symptoms arise
after 2–10 days of incubation; 3: The serious form of the disease named ‘Legionnaire’s disease’ generally arise in weakened patients (elderly,
immunocompromised, etc.) which can evolve to a lethal pulmonary infection in about 15% of cases; 4: The treatment is based on antibiotics;
5: While writing this chapter, a Legionella epidemic was raging within the north of France (Department: Pas de Calais). More than 80 cases were
registered during January 2004.
10.4 Humans get sick, age, and die!
Modern humans try to live better and longer. These
days, this desire has culminated in massive pharmaceutical and medical industries and associated
science base, as well as on going interest in alternative medicine. Unsurprisingly, some pathogens take
advantage of human illness and death, and of the
new openings provided by medical science.
10.4.1 Sickness
‘Despite a century of often successful prevention and
control efforts, infectious diseases remain an important global problem in public health, causing over
13 million deaths each year. Changes in society,
technology and the microorganisms themselves are
contributing to the emergence of new disease’ Cohen
(2000). During the twentieth century, many medical
and public health officials were optimistic that most
of infectious diseases could be eradicated. This has
patently not occurred, and indeed that the ongoing
emergence of new pathogens is a reality (Liautard
1997). Pathogens have plunged into the new ecological niches provided by new human behaviours and
customs. It would be impossible and tedious to
make an exhaustive review of these diseases,
because they are so numerous. The development of
medical technology in hospital ecosystems lead to
the development of cohorts of opportunistic
pathogens which exploit these new ecosystems.
Diseases emerging in hospital ecosystems are known
under the terminology ‘Nosocomial infections’
(hospital-acquired infections), derived from the
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Greek ‘nosokomeion’, which means hospital.
Hospitals are the source of many diseases because
patients are often immunocompromised, and
because infected people come to hospitals. The
majority of nosocomial infections have an endemic
origin (i.e. inside the hospital), where infection
comes from a microorganism present in the ecosystem, and the surgical intervention renders it infectious. In an important article, Cohen (2000) reviewed
the causes of nosocomial infections in modern medical environments. The classical case is represented
by an inoffensive bacterium that is brought by
the surgeon’s lancet into the body of a patient
and evolves to a septicaemia. Figure 10.5 illustrates
different origins of nosocomial infections where
medical tools can be incriminated. These infections
can be due to microbes that have lived on or in
(i.e. colonized) the patient for many years without
harm before healthcare procedure provides a means
of bypassing the patient’s host defences (Farr 2003).
Nosocomial infections have been known for a
long time in hospital ecosystems: Oliver Wendell
Catheter
Endoscope
2
1
Biopsy catheter
Contaminated hospital environment
Endogenous
Nosocomial infections
Exogenous
Infected patient
3
(a)
Needle (venipuncture)
(b)
4
Prosthesis: new ecosystem
Figure 10.5 Nosocomial infections.
Notes: Following an invasive surgery (i.e. through the skin as illustrated in 1, 2, 3, for example), a patient can be infected by germs coming from an:
Endogenous origin: patient is infected by its own germs following a surgical act and/or because he displays a particular weakness. For example, a patient
under artificial breathing can develop pneumonia from a germ of its own digestive tract, which can go up to the respiratory ways. The same phenomenon
can be observed for an urinary infection from an urinary probe carrier.
Exogenous infection: Cross infections transmitted from a patient to another through hand contacts or medical tools. These infections can be originated
from the germs inhabiting hospital workers, or linked to the contamination of the hospital environment (water, air, material, foods, etc.).
Prosthesis constitutes new ecosystems for pathogens. The figure shows a knee prosthesis (4): (a) before; and (b) after.
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Holmes published a paper on this topic as early as
1843. Nosocomial infections can be directly linked
to medical treatment, or can simply occur during
hospitalization, independently of any medical act.
They concern patients, but also workers present
in this ecosystem. They can occur because the
immune system is busy fighting some other chronic
illness, or for people who are immunocompromised. People can be immunocompromised from
certain diseases (e.g. AIDS), certain medications
(e.g. immunosuppressants or chemotherapy), surgical recovery, or other serious medical complaints
that limit the person’s ability to fight against these
infections (Berche et al. 2000).
These infections can spread by endogenous
or exogenous ways (Fig. 10.5). Many types of
pathogens are involved, including fungal infections
(e.g. Candida, Aspergillus, Fusarium), bacterial and
viral pneumonia (e.g. influenza, Staphylococci,
Pseudomonas) which can be found in different
organs, giving rise to urinary tract infections, surgical site infections, respiratory tract infections, blood
stream infections, skin infections, gastrointestinal
tract infections, central nervous system infections,
and so on. Numerous surgical acts can initiate
nosocomial infections, these fall into three main
types: (i) urogenital probes lead to urinary infections, (ii) catheters are sources of systemic and local
bacterial and viral infections, and (iii) artificial
breathing systems are responsible of pulmonary
infections. For a lead into the extensive literature
on nosocomial infections see Arnow et al. (1993),
Scheckler et al. (1998), Lucet (2000), Lemaitre
and Jarlier (2000), Korinek (2000), and Joly and
Astagneau (2000).
The frequency of nosocomial infections in France
is typical of industrialized countries, with about 7%
of hospitalized patients developing a nosocomial
infection. In other countries it ranges from from 5%
to 12%. In the United States, more than 2 million
cases of nosocomial infections have been reported,
leading to about 80,000 deaths and to 8000 additional days in hospital for 1000 infected patients, all
at a cost of $US5 billion dollars in 1985 (Wenzel
1985; Haley 1991).
In this section on human sickness, we can illustrate the Machiavellianism of pathogens exploiting
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a human health problem: drug addiction. Many
pathogens from viruses to worms use insect as
vectors in order to infect new hosts. In the same way,
we could do a comparison with medical tools that
pathogens use as vectors. The best and saddest
example could be the syringe which represents
a wonderful vector for pathogens to pass from host
to host. A non sterilized syringe represents a very
efficient ecosystem exploited by many pathogens.
One terrible recent example was provided by HIV
and drug addiction. The HIV virus can be passed
through different venous injections from different
individuals sharing the same syringe. Unfortunately,
this problem does not only occur within drug
addicts; nurses in hospital have been contaminated
by this parasite when taking a blood sample from
infected patients. AIDS is one of the major diseass
at the beginning of the twenty-first century, and we
have to keep in mind the public scandal which
occurred in France at the end of the twentieth
century with contaminated HIV blood. Indeed,
haemophiliacs need recurrent blood transfusions,
and before the use of warmed blood elements, many
of them were infected by HIV through the needle
which served to transfuse them (Fig. 10.5). Most of
them died, and this scourge continues to kill a lot of
people in the world.
10.4.2 Ageing
Modern humans live longer, at least in industrialized countries, where the number of the elderly is
rapidly increasing (Morris and Potter 1997). This
leads to an increasingly large group of hosts ripe for
exploitation. For example, ageing results in senescence of the gut-associated lymphoid tissue, and
decreasing in gastric acid secretion (Feldman et al.
1996). The consequences of these physiological
disturbances lead to an increase of susceptibility to
pathogens. Indeed, as a low pH of the stomach
represents an important barrier to entry of enteric
pathogens, reduction in gastric acidity can increase
the susceptibility to infection by these pathogens
(Morris and Potter 1997). The communal living
environment of some elderly, exacerbated by problems such as incontinence, further creates an
habitat in which enteric and food-borne pathogens
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can spread rapidly (Benett 1993). In a study
between 1968 and 1979 in the United States, Blaser
and Feldman (1981) showed that the frequency of
Salmonella bacteremia increased dramatically in the
elderly compared with other age groups. Salmonella
infections increase the risk of death, and elderly are
often immunocompromised and they are assisted
by a large cohort of medications. This treatment
undeniably leads to the selection of drug resistance
in many categories of pathogens. The grouping of
patients in ‘elderly care homes’ may constitute production units of ‘pathogen resistant ecosystems’,
which will represent a new and complex public
health problem as the population ages. We expect
that pathogens produced in these ecosystems,
many of which may be drug resistant, will spill out
to attack other age groups of the population
(i.e. babies, toddlers, and children)? To our knowledge, policies have not yet considered this ecological problem. It is well known in evolutionary
parasitology that an increase in the number of
susceptible hosts can have dramatic consequences
for the spread of pathogens in the whole population
(Bird Influenza Virus below).
10.4.3 Death
Even if human have largely improved health care
and have lengthened life expectancy, particularly in
industrialized countries, death always occurs.
Humans worship death and we can observe a lot of
flower vases in some cemeteries. These vases can
constitute ideal ecosystems for the development of
different mosquito species larvae. In a very interesting paper, Lancaster et al. (1999) related the invasion of Ae. albopictus into an urban encephalitis
focus, where flower vases ecosystems found in
cemeteries could play an important role.
Elsewhere, O’Meara et al. (1995) investigated the
competition between Aedes aegypti and Ae. albopictus in a US cemetery named Rose Hill, and showed
that until the summer of 1990, only Ae. aegypti
inhabited vases at Rose Hill. Ae. albopictus was first
collected that summer and by 1994, had become the
most prevalent species (i.e. greatest percentage of
vases occupied). Juliano (1998) sampled three
cemeteries in Southern Florida where Aedes inhabit
water-filled stone cemetery vases. From manipulative field experiments, he analysed the mechanisms
involved in the competition between Ae. aegypti
and Ae. albopictus. He showed that, at least at the
three sites tested, Ae. albopictus was more competitive than Ae. aegypti. This invader superiority was
attributed to better resource acquisition in these
ecosystems. Knowing that these mosquito species
are vectors of different pathogenic viruses, these
cemetery ecosystems can play an undeniable role in
mosquito transmitted diseases, at least in the area
concerned.
10.4.4 Surgical progress
Like different mechanical parts of our car, many
organs of our body can be replaced by better functioning parts. Xenotransplantation is the graft
(i.e. skin, tissue) or the transplant (i.e. organ) into
humans of tissue or organs from animals (Wadman
1996). Xenotransplantation seems a very real possibility now that the generation of transgenic
pigs as potential organ donors for humans has
been achieved. Baboons are also likely to be used,
especially so for bone marrow grafting. But, both
baboons and pigs may silently harbour a great variety of viruses belonging mostly but nor exclusively
to the Herpesviridae, Retroviridae, and Papoviridae
families. All these viruses are potentially able to
infect deeply immunocompromised patients. This
may lead to the emergence of deadly viral infections, the so-called ‘xenozoonosis’, among the
recipients and/or the general population (Chastel
1996). Indeed, the majority of viruses that emerged
during these last 30 years displayed a zoonotic
(mainly simians) origin (Morse and Schluederberg
1990). For example, the Herpesvirus simiae , specific
to asian cerpothitecicidae of the genus Macaca and
where it seems to be a largely benign virus,
becomes very dangerous for human when injected
by biting or by accidental injection by infected
syringe or needle (Artensein et al. 1991). DNAs
represent a well-established molecular species
ecosystem where a large number of selfish DNAs
(including number of viruses) are evolving and
pass through generations. Each species harbours its
own selfish DNAs, and they constitute, for
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example, a large part of the human genome (De
Meeûs et al. 2003). Therefore, transmission of virus
through grafts is confirmed, and allografts were
reported to be at the origin of primary infections by,
at least, the cytomegalovirus, Epstein–Barr virus,
VIH, and hepatitis C (Chastel 1998). We could be
thus confronted to a new virulent variant of these
viruses or to a genetic matching between close
human and simians viruses (i.e. Herpesvirus,
Retrovirus). We cannot exclude the possibility of an
outbreak of a genetic chimera between human and
animal viruses, or of the ‘complementation’ of a
defective virus. Xenotransplants can come from
transgenic animal in order to avoid graft rejection
by human recipient. ‘I view xenograft tissues as
essentially very complex vectors for shuttling new
viruses in humans’ (Allan 1995).
Prostheses are another example of surgical
progress. The addition of exogenous material leads
to the establishment of new ecosystems inside
the body (Fig. 10.5). These new niches can be
colonized by pathogens. For example, prosthetic
joints, prosthetic implants, and vascular prosthetic
materials are a ‘nest’ for many pathogens such
as group C Streptococcus, Staphylococcus epidermidis,
Staphylococcus aureus, Mycobacterium tuberculosis,
Histoplasma capsulatum (Gillespie 1997; Kleshinski
et al. 2000).
use) and contraceptive methods (i.e. Intra-Uterine
contraceptive Devices—IUDs or coil). The insertion
of tampons or coils in female genital systems represents a new opportunity for pathogens. Urinary
tract infections of women are common, and a
source of considerable expense. The possibility that
tampon usage is a risk factor for recurrent urinary
tract infection has not been studied in detail, but it
has been associated with bacterial vaginosis. The
tampon may facilitate the spread of bacteria from
the vagina to the urethra and bladder (Doran 1998).
Elsewhere, it was thought that IUD infections
spread through lymphatic canals to produce a
perisalpingitis similar to that of postabortal or
postpartum infections. Even if it was not demonstrated that IUDs are directly responsible of these
infections, their role remains to be determined
(Schwarz 1999).
10.4.5 Hygienic progress
10.5.1 Tinned food
Polio was almost unknown until the dramatic
epidemics that terrorised the developed countries
in the twentieth century. This terror led to irrational
responses, such as aggression to immigrants of
shantytowns. Before hygiene was common, infants
were safely immunized against polio by maternal
milk. However, once hygiene standards were high
in developed countries, individuals were first
exposure to polio occured at older ages, when the
clinical complications are likely. Thus, changing
hygiene habits has allowed the poliovirus to
the exploitation of new habitats, with dramatic
consequences for the host (Schlein 1998; Seytre and
Schaffer 2004).
Medical progress has led to women being
attacked by pathogens due to menses (i.e. tampon
A major problem to which human populations
were and are still confronted is to food preservation. Different methods of food conservation were
developed in human societies, but two of them are
the more used, at least in industrialized countries:
tinned and cooled food.
Listeriosis, a serious infection caused by food
contaminated by the bacterium Listeria monocytes,
has recently been recognized as an important
health problem in the United States and European
countries (Lorber 1997; Silver 1998). Listeriosis is a
disease that is enhanced by alimentary progress.
This bacterium is frequently found in soil and
water, and becomes pathogenic for human when
ingested at high densities. Naturally contaminated
food never presents dangerous densities of this
10.5 Human need to eat!
Life, reduced to its simplest expression, could be
caricatured through two main functions for each
individual in each plant and animal species: survival and reproduction. Food is the fuel for this, but
eating is not without risk. Our new food habitats
have opened up new niches for many pathogens.
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bacterium, but this pathogen experiences an
increase of its population demography at low temperatures. Refrigerators constitute a favourable
ecosystem for these bacterial populations where
they can reach the infectious quantity dose for
human.
Human brucellosis or ‘Bang’s disease’ which was
discovered a century ago remains poorly known
and difficult to treat. Pathogens responsible for the
disease are bacteria belonging to the genus Brucella,
a strictly aerobic coccobacillus. Brucella can enter
the body via the skin, respiratory tract, or digestive
tract. Once there, this intracellular organism can
enter the blood and the lymphatic canals where it
multiplies inside the phagocytes. The disease
spreads through animal contacts or contaminated
food, especially cheese! Cheese permits milk to be
preserved, and several hundred of people are
infected each year in France. The disease causes
nausea, meningitis, hepatitis, and miscarriages
(Straight and Martin 2002).
Botulism is a food-borne disease; the agent of the
disease is an anaerobic bacteria Clostridium botulinium with a spore-forming rod that produces a
neurotoxin. The spores are heat-resistant and can
survive in foods that are incorrectly or minimally
processed. The disease is caused by the neurotoxin
produced by C. botulinium that is present in the
food (Smith and Sugiyama 1988). The organism
and its spores are widely distributed in nature
(e.g. cultivated and forest soils, coastal waters, gut
of fish and mammals, gills and viscera of crabs and
other shellfishes), but the types of foods involved in
botulism vary according to regional food preservation and eating habits. Almost any type of food that
is not too acidic (pH above 4.6) can support the
growth and toxin production of C. botulinium.
Botulinal toxin has been evidenced in a considerable variety of foods, such as canned corn, soups,
ham, sausage, smoked, and salted fish. The incidence of the disease is low, but the mortality is high
if not immediately and properly treated.
10.5.2 Intensive farming
High intensity farming has been very good at producing large amounts of cheap food, but has also
opened up new parts of the human–pathogen
ecosystem. Salmonellosis is one of the most common food-borne illness causing enteric infections in
developed countries. The pathogens are bacteria
(Salmonella) which consist of a range of very related
bacteria, many of which are pathogenic to humans
and animals (Thorns 2000). The strains which are
implicated in the diseases are generally different
serovars of Salmonella enterica that caused diseases
of the intestine, as suggested by their name. For
example, S. enterica serovar typhi is the causative
agent of typhoid fever. It is very common in developing countries, where it causes a serious and often
fatal disease. Salmonella bacteria primarily invade
the wall of the intestines causing inflammation and
damage. Infection can spread in the body through
the bloodstream to other organs such as liver,
spleen, lung, joints, placenta, or foetus, and the
membrane surrounding the brain. Toxic substances
produced by bacteria can be released and affect the
rest of the body. Salmonella has evolved mechanisms to escape our immune system (Olsen et al.
2001). In the liver, bacteria can grow again, and be
released back into the intestine. S. enterica serovar
enteritidis has become the single most common
cause of poisoning in the United States in the last
20 years. Salmonella are found in contaminated
food, with recent increases in the number S. enteritidis
a consequence of mass production chicken farms.
When tens or hundreds of thousands of chickens
live together, die together and are processed
together, a Salmonella infection can rapidly spread
throughout the whole food chain, and hence
Salmonella can be rapidly dispersed among million
of people.
Changed farming practices have also led to
new opportunities for non-food-borne human
pathogens. In the Asillo zone, located at a very high
altitude of 3910 m in the Peruvian Altiplano, high
levels of human infection by Fasciola hepatica
(i.e. the liver fluke) were linked to man-made irrigation zones. Man-made irrigation areas are built
only recently to which both liver fluke and lymnaeid snails (i.e. the first intermediate host of the
liver fluke) have quickly adapted. Such man-made
water resources in high altitude of Andean countries dangerously inflate the parasitic risk, because
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the lack of drinking water and running water inside
dwellings forces inhabitants to obtain water from
irrigation canals and drainage channels (Esteban
et al. 2002). Elsewhere, it is largely recognized that
a significant amount of malaria transmission in
Africa and Madagascar is due to human activities.
Modifications of the environment resulting from
land use often create or alter habitats for mosquito
vectors, and may indirectly affect parasite development rates, and the lifespan of mosquito (Service
1991; Ault 1994; Coluzzi 1994).
Marine ecosystems are also on the danger list due
to pollution and aquaculture which modify all
parameters of natural equilibrium. The organic pollution exerts both oppressing and stimulating influences, with industrial waste depressing the
formation and function of parasite systems. Some
current aquaculture practices are environmentally
benign, others, especially those in some of the
fastest growing portions of the industry, can
degrade water quality, transmit diseases to wild
populations, disrupt marine ecosystems, and
spread invasive parasites and pathogens species
(Maender 2002; Young 2003, see also Chapter 7).
We think that it is now important to present a
current very deep problem which links public and
veterinary health. At the time we are writing this
chapter at the beginning of 2004, public opinion
and World Health Organization is strongly focused
on two animal zoonotic diseases which have arisen
recently, particularly in Asia. ‘The terror of the
unknown is seldom better displayed than by the
response of a population to the appearance of an
epidemic, particularly when the epidemic strikes
without apparent cause’. This quote from Kass
(1977) concerned the emergence of legionnaires’
disease, and it well describes public response to
the recent emergence of an atypical pneumonia
named as Severe Acute Respiratory Syndrome
(SARS). SARS was first recognized in the
Guangdong Province of China, in November 2002.
Subsequent to its introduction in Hong Kong in
mid-February 2003, the virus spread to more than
thirteen countries and caused disease across five
continents. According to the World Health
Organisation (WHO) in January 2004, a cumulative
total of eight thousand SARS cases with more than
167
800 deaths had been reported. A novel coronavirus
was identified as the human etiological agent of
SARS, causing a similar disease in cynomolgous
macaques (Peiris et al. 2003). Because cases where
SARS was first diagnosed occurred in restaurant
workers handling wild mammals and exotic food,
scientists focused on wild animals recently captured and marketed for consumption. Their work
provides evidence that SARS shifts from animals to
humans, possibly frequently (Guan et al. 2003).
Elsewhere, Stanhope et al. (in press) have confirmed this host shift, because they could identified
that SARS-CoV has a recombinant history with
lineages of types I and III virus, concomitant
with the reassortment of bird and mammalian
coronaviruses. Food marketing trades could thus
provide the opportunity animal ScoV-like viruses
to amplify and to be transmitted to new hosts,
including humans. Even if the natural reservoir is
not clearly identified, market animals (civets, raccoon dog, and ferret badgers for example) might
be compatible hosts that increase the opportunity
for transmission of the virus to humans. Markets
constitute thus man-made ecosystems favourable
to a new set of pathogenic agents. Thousand of
these aforesaid animal species have been slaughtered as a preventive measure. But, is it the most
efficient solution?
The Avian Influenza outbreak which is currently
raging in south east Asia is related to SARS only in
demonstrating how the so-called zoonotic diseases
in animals can become a threat to human health. It
clearly illustrates how man-made intensive farming
ecosystems can represent spring boards for new
pathogens. Highly pathogenic avian influenza
A viruses of subtypes H5 and H7 belong to the
Orthomyxoviridae family, and are the causative
agent of fowl plague in poultry. Type A influenza
viruses are those which affect humans, but also
pigs, horses, and some marine mammals (whales
and seals). There are three types (A, B, and C) of
influenza viruses, depending on the antigens
detected in the virus capsid. The antigens that are
used to recognize the different viruses belong to
two kinds of glycoproteins, hemagglutinin (HA),
and neuramidase (NA). There are fifteen different
HA antigens (H1 to H15) and nine different NA
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antigens (N1 to N9) for influenza A. Human
disease historically has been caused by three
subtypes of HA (H1, H2, and H3) and two subtypes
of NA (N1 and N2), which were responsible for
million of deaths around the world, through different pandemics. All known subtypes of influenza A
can be found in birds, but only subtypes H5 and H7
have caused severe disease outbreaks in bird populations (Fouchier et al. 2004). Figure 10.6 illustrates
the life cycle and possible routes taken by these
pathogens; migratory birds and waterfowl are
thought to serve as reservoir hosts for influenza A
virus in nature (Murphy and Webster 1996), but
waterfowls generally do not suffer from the disease
when infected with avian influenza.
The viruses easily circulate among birds worldwide as they are very contagious for birds, and can
be deadly, particularly for domesticated birds like
chickens and turkeys. The disease spreads
rapidly within poultry flocks and between farms.
Direct contact of domestic flocks with wild migratory waterfowls has been implicated as a frequent
cause of epidemics, and live bird markets are implicated in the spread of the disease. Avian influenza
A virus may initiate new pandemics in humans
because the human population is serologically
naive toward most HA and NA subtypes (Fouchier
et al. 2004). Until recently, it was considered that
pigs were the obligate intermediate host for transmission of these virus types to humans (Yasuda et
al. 1991; Webster 1997, Fig. 10.6). Past influenza
pandemics have led to high levels of illness, death,
social disruption and economic loss (Fig. 10.6), but
in general, avian influenza viruses do not replicate
efficiently or cause disease in humans (Bear and
Webster 1991). However, the highly pathogenic
influenza virus subtype H5N1, first documented
in Hong Kong in 1997, was transmitted in 2003
from bird to humans, and was responsible for
a very serious outbreak, the seriousness of which is
still unclear at time of writing. Nevertheless, this
epidemic is an illustration of how intensive poultry
farming ecosystems (i.e. increasing host density
to increase food productivity) are responsible for
these new outbreaks, at least in the countries
where this influenza H5N1 virus finds its origin
(Fig. 10.6).
10.5.3 But how can viruses of high and low
virulence coexist?
This is a case of a classical question in evolutionary
biology: what conditions are required to maintain
polymorphism (genetic and/or phenotypic variability), in space and time, within and among
populations of all kind of species? Literature on the
topic is rich (e.g. De Meeüs et al. 1993 and 1995;
De Meeüs and Renaud 1996 for examples). We will
not attempt here to make a review on this topic, but
in their paper published in 2004, Boots, Hudson,
and Sasaki developed a theoretical model to envisage the conditions for maintenance and spreading
of low versus high virulent type of pathogens
(e.g. viruses). The model clearly shows that large
shifts in pathogen virulence are related to host
population structure (i.e. demography and genetic).
Poultry flock structures managed by humans
represent new ecological and demographic configurations for the evolution and emergence of new
virulent pathogen strains, which enter more and
more in contact with human populations.
Given the increasing long-distance movement of people
and domestic animals around the modern world, our
results have important implications for emerging diseases
in general. Recombination among avirulent (and therefore
possibly previously undetected) strains of viruses and
other pathogens may produce new virulent strains that
may spread through vertebrate host populations because
they have shifted to a new evolutionary stable state.
(Boots et al. 2004)
What is happening with the current influenza
outbreak has been clearly predicted by theoretical
population biology models. This stresses the need
there is that such approaches should be taken now
into account in future public and veterinary health
control.
Pathogens and parasites can use different manmade ecosystems to spread and threaten human’s
health. Indeed, as illustrated in the case of influenza
virus, the pathogen can first exploit the intensive
farming processes (i.e. food production) in order
to emerge and rapidly infect humans (Fig. 10.6),
and second, hitch-hike the man-made ‘travel ecosystems’ (i.e. plane, boat, or train) to spread among
populations and become pandemic (Fig. 10.2).
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1
2
N1
H5
4
3
A
B
Figure 10.6 Avian influenza: (a) infecting routes and (b) geographical outbreaks in 2004 and the Avian influenza virus.
Notes: (a) Waterfowl are thought to be the natural reservoir of Avian influenza A viruses (1). Viruses replicate in the intestines as well as the respiratory
tract of birds.
During migratory processes of birds, poultry flocks become infected when contacts between them and naturally infected birds are established. In the 2004
outbreak, very large quantities of virus were excreted in the faeces of infected farming birds, resulting in widespread contamination of the environment
(2). This presence of numerous H5N1 subtype created one of the most important risks for human exposure and subsequent infection.
Some findings support the hypothesis that the pig was a ‘mixing vessel’, able to produce new virus subtypes by genetic reassortment that can infect
humans. Until recently, it was supposed that pigs were obligatory intermediate hosts for human infections (3). Nevertheless, epizoonose of Avian Influenza
in different Asian countries in 2004 confirmed the possibility of direct human infection from birds, via the H5N1 Influenza virus subtype (4). Indeed, if Avian
Influenza viruses lack the receptors needed to infect mammals efficiently, the infection of humans observed during the 2004 and two previous H5N1
outbreaks demonstrates that transmission from birds to mammals, including humans, can occur despite the lack of receptors. (b) The influenza
outbreak in 2004 affected more than ten Asian countries.
From the 20 February 2004, Thai authorities reported that 147 patients were admitted in the hospital since the beginning of the zoonotic outbreak, and
eight died. The main problem for all countries around the world is that this Asian influenza outbreak became pandemic. There were three pandemics in the
twentieth century. All of them spread worldwide within one year:
– 1918–19: ‘Spanish flu’ [H1N1]: 20–50 million people died worldwide. Nearly half of those who died were young, and healthy adults.
– 1957–58: ‘Asian flu’ [H2N2]: First identified in China, the Asian flu spread in the United States and caused about 70,000 deaths.
– 1968–69: ‘Hong Kong flu’ [H3N2]: First identified in Hong Kong, the virus spread in the United States and caused about 35,000 deaths.
More than seven billion poultry were slaughtered in infected Asian countries which suggest the farming of billions of bird in this geographic area. This
demographic situation is favourable for (i) the emergence and the spread of highly virulent strains of pathogens within and between stock breeding,
and (ii) the transfer between host species, including humans.
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In front of such processes, we do not know which
zoonoses will become important in public health in
the future, and we must be vigilant over the
emergence of new pathogens.
10.6 Concluding remarks
It was not our intention to produce an exhaustive
review of all situations where pathogens and parasites found new infectious routes associated with
human customs, development, and technology, and
we are conscious of many gaps (for instance,
Western beds provide an excellent ecosystem for
ectoparasites such as lice, fleas, ticks, sarcoptes, bed
bugs, etc.). But our goal was to present some
aspects which we believe will become more and
more topical given current trends. We believe
future key questions will be how societies could
and should manage (i) population ageing,
(ii) need of food access, (iii) earth demographic
growth, (iv) people density and urbanization,
(v) new technical and medical tools. This is a challenge for which we must get prepared. Pathogens
are everywhere and can adapt to a wide panel of
environments (even computers). Indeed, we may
be just at the beginning of the evolution of
pathogens and parasites evolution in our biosphere
ecosystem.